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Microbial decomposition of crustacean shell for production of bioactive metabolites and study of its fertilizing potential

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Abstract

Crustacean shell waste disposal is considered as biggest problem in seafood processing centers. Incineration and landfilling are the commonest ways of disposal of the waste which causes environmental pollution. Microbial bio-conversion is one of the promising approaches to minimize the wastes by utilizing the same for deriving different value added metabolites. In this perspective, chitinase- and protease-producing bacterial strains were isolated from shrimp culture pond, and the potent isolate was subsequently identified as Alcaligenes faecalis SK10. Fermentative optimization of the production of chitinase (85.42 U/ml), protease (58.57 U/ml), and their catalytic products, viz., N-acetylamino sugar (84 μg/ml) and free amino acids (112 μg/ml), were carried out by utilizing shrimp and crab shell powder as principal substrate. The fermented hydrolysate (FH) was subsequently applied to evaluate its potential to be a candidate fertilizer for the growth of leguminous plant Pisum sativum and Cicer arietinum, and the results were compared with chitin, chitosan, and commercial biofertilizer amended group. The results revealed that FH have paramount potential to improve plants morpho-physiological parameters like stem and root length, chlorophyll, cellular RNA, protein content, and soil physico-chemical parameters like total nitrogen, magnesium, calcium, phosphorus, and potassium significantly (p < 0.05). Moreover, the application of FH also selectively encouraged the growth of free-living nitrogen-fixing bacteria, Rhizobium, phosphate-solubilizing bacteria in the soil by 4.82- and 5.27-, 5.57- and 4.71, and 7.64- and 6.92-fold, respectively, in the rhizosphere of P. sativum and C. arietinum, which collectively is a good sign for an ideal biofertilizer. Co-supplementation of FH with commercial PGPR-biofertilizer significantly influenced the morpho-physiological attributes of plant and physico-chemical and microbial attributes of soil. The study validated proficient and sustainable utilization of fermented hydrolysate of waste crustacean shell as biofertilizer.

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References

  • Aditya B, Neena P, Chauhan PS, Cheema BS, Naveen G (2014) Studies on alkaline-thermostable protease from an alkalophilic bacterium: production, characterization and applications. Int J Environ Sci 5(2):353–371

    Google Scholar 

  • Akhir SM, Abd-Aziz S, Salleh MM, Rahman RA, Illias RM, Hassan MA (2009) Medium optimisation of chitinase enzyme production from shrimp waste using Bacillus licheniformis TH-1 by response surface methods. Biotechnology 8(1):120–125

    Article  CAS  Google Scholar 

  • Arnold ND, Brück WM, Garbe D, Brück TB (2020) Enzymatic modification of native chitin and conversion to specialty chemical products. Mar Drugs 18(2):93

    Article  CAS  Google Scholar 

  • Benhabiles MS, Salah R, Lounici H, Drouiche N, Goosen MF, Mameri N (2012) Antibacterial activity of chitin, chitosan and its oligomers prepared from shrimp shell waste. Food Hydrocoll 29(1):48–56

    Article  CAS  Google Scholar 

  • Berger LR, Stamford NP, Santos CERS, Freitas ADS, Franco LO, Stamford TCM (2013) Plant and soil characteristics affected by biofertilizers from rocks and organic matter inoculated with diazotrophic bacteria and fungi that produce chitosan. J Soil Sci Plant Nutr 13(3):592–603

    Google Scholar 

  • Chakrabarti R (2002) Carotenoprotein from tropical brown shrimp shell waste by enzymatic process. Food Biotechnol 16(1):81–90

    Article  CAS  Google Scholar 

  • Chakrabortty S, Bhattacharya S, Das A (2012) Optimization of process parameters for chitinase production by a marine isolate of Serratia marcescens. Int J Pharm Biol Sci 2(2):8–20

    CAS  Google Scholar 

  • Chang WT, Chen CS, Wang SL (2003) An antifungal chitinase produced by Bacillus cereus with shrimp and crab shell powder as a carbon source. Curr Microbiol 47(2):0102–0108

    Article  CAS  Google Scholar 

  • Chauhan PS, Bharadwaj A, Puri N, Gupta N (2014) Optimization of medium composition for alkali-thermostable mannanase production by Bacillus nealsonii PN-11 in submerged fermentation. Int J Curr Microbiol App Sci 3(10):1033–1045

    Google Scholar 

  • Chen JK, Shen CR, Yeh CH, Fang BS, Huang TL, Liu CL (2011) N-acetyl glucosamine obtained from chitin by chitin degrading factors in Chitinbactert ainanesis. Int J Mol Sci 12(2):1187–1195

    Article  CAS  Google Scholar 

  • Das G, Prasad MP (2010) Isolation, purification and mass production of protease enzyme from Bacillus subtilis. Int Res J Microbiol 1(2):26–31

    Google Scholar 

  • Dénarié J, Debellé F, Promé JC (1996) Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu Rev Biochem 65(1):503–535

  • Dutta P, Deb A, Majumdar S (2016) Optimization of the medium for the production of extracellular amylase by the Pseudomonas stutzeri ISL B5 isolated from municipal solid waste. Int J Microbiol. https://doi.org/10.1155/2016/4950743

  • El Hadrami A, Adam LR, El Hadrami I, Daayf F (2010) Chitosan in plant protection. Mar Drugs 8(4):968–987

    Article  CAS  Google Scholar 

  • Fatima B, Zahrae MF, Razouk R (2018) Chitin/Chitosan’s bio-fertilizer: usage in vegetative growth of wheat and potato crops. In: Dongre R (ed) Chitin-chitosan: myriad functionalities in science and technology. IntechOpen, pp 331–353. https://doi.org/10.5772/intechopen.75208

  • Frąc M, Hannula SE, Bełka M, Jędryczka M (2018) Fungal biodiversity and their role in soil health. Front Microbiol 9:707

    Article  Google Scholar 

  • Gogoi M, Basumatary M (2018) Estimation of the chlorophyll concentration in seven citrus species of Kokrajhar district, BTAD, Assam, India. Trop Plant Res 5:83–87

    Article  Google Scholar 

  • Gupta R, Beg Q, Lorenz P (2002) Bacterial alkaline proteases: molecular approaches and industrial applications. Appl Microbiol Biotechnol 59(1):15–32

    Article  CAS  Google Scholar 

  • Halder SK, Mondal KC (2018) Microbial valorization of chitinous bioresources for chitin extraction and production of chito-oligomers and N-acetylglucosamine: trends, perspectives and prospects. In: Microbial Biotechnology. Springer, Singapore, pp 69–107

    Chapter  Google Scholar 

  • Halder SK, Maity C, Jana A, Pati BR, Mondal KC (2012) Chitinolytic enzymes from the newly isolated Aeromonas hydrophila SBK1: study of the mosquitocidal activity. BioControl 57(3):441–449

    Article  CAS  Google Scholar 

  • Halder SK, Maity C, Jana A, Das A, Paul T, Mohapatra PK, Pati BR, Mondal KC (2013) Proficient biodegradation of shrimp shell waste by Aeromonas hydrophila SBK1 for the concomitant production of antifungal chitinase and antioxidant chitosaccharides. Int Biodeterior Biodegradation 79:88–97

    Article  CAS  Google Scholar 

  • Hu X, Tian Z, Li X, Wang S, Pei H, Sun H, Zhang Z (2020) Green, simple, and effective process for the comprehensive utilization of shrimp shell waste. ACS Omega 5(30):19227–19235

    Article  CAS  Google Scholar 

  • Husseiny SM, Halamsh FA, Said RM (2008) Shrimp shell as an inexpensive substrate for protease production by Pseudomonas Alcaligenes in submerged fermentation. New Egypt J Microbiol 20:291–302

    Google Scholar 

  • Itelima JU, Bang WJ, Onyimba IA, Sila MD, Egbere OJ (2018) Bio-fertilizers as key player in enhancing soil fertility and crop productivity: a review. Dir Res J Agri Food Sci 6(3):73–83

  • Jholapara RJ, Mehta RS, Sawant CS (2013) Optimization of cultural conditions for chitinase production from chitinolytic bacterium isolated from soil sample. Int J Pharm Bio Sci 4(2):464–471

    CAS  Google Scholar 

  • Karunya SK, Reetha D, Saranraj P, Milton DJ (2011) Optimization and purification of chitinase produced by Bacillus subtilis and its antifungal activity against plant pathogens. Int J Pharm Biol Arch 2(6):1680–1685

  • Khan MS, Ahmad E, Zaidi A, Oves M (2013) Functional aspect of phosphate-solubilizing bacteria: importance in crop production. In: Bacteria in agrobiology: Crop productivity. Springer, Berlin, Heidelberg, pp 237–263

    Chapter  Google Scholar 

  • Kour D, Rana KL, Yadav AN, Yadav N, Kumar V, Kumar A, Saxena AK (2019) Drought-tolerant phosphorus-solubilizing microbes: biodiversity and biotechnological applications for alleviation of drought stress in plants. In: Plant growth promoting rhizobacteria for sustainable stress management. Springer, Singapore, pp 255–308

    Chapter  Google Scholar 

  • Kuddus M, Ahmad IZ (2013) Isolation of novel chitinolytic bacteria and production optimization of extracellular chitinase. J Genet Eng Biotechnol 11(1):39–46

    Article  Google Scholar 

  • Lee YS, Kim KY (2015) Statistical optimization of medium components for chitinase production by Pseudomonas fluorescens strain HN1205: role of chitinase on egg hatching inhibition of root-knot nematode. Biotechnol Biotechnol Equip 29(3):470–478

    Article  CAS  Google Scholar 

  • Liang TW, Chen YY, Pan PS, Wang SL (2014) Purification of chitinase/chitosanase from Bacillus cereus and discovery of an enzyme inhibitor. Int J Biol Macromol 63:8–14

    Article  CAS  Google Scholar 

  • Limpanavech P, Chaiyasuta S, Vongpromek R, Pichyangkura R, Khunwasi C, Chadchawan S, Lotrakul P, Bunjongrat R, Chaidee A, Bangyeekhun T (2008) Chitosan effects on floral production, gene expression, and anatomical changes in the Dendrobium orchid. Sci Hortic 116(1):65–72

    Article  CAS  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    Article  CAS  Google Scholar 

  • Mathew GM, Mathew DC, Sukumaran RK, Sindhu R, Huang CC, Binod P, Sirohi R, Kim SH, Pandey A (2020) Sustainable and eco-friendly strategies for shrimp shell valorization. Environ Pollut 267:115656

  • Mechri S, Sellem I, Bouacem K, Jabeur F, Laribi-Habchi H, Mellouli L, Hacène H, Bouanane-Darenfed A, Jaouadi B (2020) A biological clean processing approach for the valorization of speckled shrimp Metapenaeus monoceros by-product as a source of bioactive compounds. Environ Sci Pollut Res 27:15842–15855

    Article  CAS  Google Scholar 

  • Nagpure A, Choudhary B, Gupta RK (2014) Chitinases: in agriculture and human healthcare. Crit Rev Biotechnol 34(3):215–232

    Article  CAS  Google Scholar 

  • Natsir H, Patong AR, Suhartono MT, Ahmad A (2010) Production and characterization of chitinase enzymes from sulili hot spring in south Sulawesi, Bacillus sp. HSA, 3-1a. Indo J Chem 10(2):256–260

    Article  Google Scholar 

  • Nelson DW, Sommers LE (1980) Total nitrogen analysis of soil and plant tissues. J Assoc Off Anal Chem 63(4):770–778

    CAS  Google Scholar 

  • Nustorova M, Braikova D, Gousterova A, Vasileva-Tonkova E, Nedkov P (2006) Chemical, microbiological and plant analysis of soil fertilized with alkaline hydrolysate of sheep’s wool waste. World J Microbiol Biotechnol 22(4):383–390

    Article  Google Scholar 

  • Pornpienpakdee P, Singhasurasak R, Chaiyasap P, Pichyangkura R, Bunjongrat R, Chadchawan S, Limpanavech P (2010) Improving the micropropagation efficiency of hybrid Dendrobium orchids with chitosan. Sci Hortic 124(4):490–499

    Article  CAS  Google Scholar 

  • Priya CS, Jagannathan N, Kalaichelvan PT (2011) Production of chitinase by Streptomyces hygroscopicus VMCH2 by optimisation of cultural conditions. Int J Pharm Bio Sci 2(2):210–219

    CAS  Google Scholar 

  • Rabea EI, Badawy MET, Stevens CV, Smagghe G, Steurbaut W (2003) Chitosan as antimicrobial agent: applications andmode of action. Biomacromolecules 4:1457–1465

    Article  CAS  Google Scholar 

  • Reissig JL, Strominger JL, Leloir LF (1955) A modified colorimetric method for the estimation of N-acetylamino sugars. J Biol Chem 217(2):959–966

    Article  CAS  Google Scholar 

  • Sedaghat F, Yousefzadi M, Toiserkani H, Najafipour S (2017) Bioconversion of shrimp waste Penaeus merguiensis using lactic acid fermentation: An alternative procedure for chemical extraction of chitin and chitosan. Int J Biol Macromol 104:883–888

    Article  CAS  Google Scholar 

  • Shamshina JL, Oldham T, Rogers RD (2019) Applications of Chitin in Agriculture. In: Sustainable Agriculture Reviews, vol 36. Springer, Cham, pp 125–146

    Google Scholar 

  • Shanmugaiah V, Mathivanan N, Balasubramanian N, Manoharan PT (2008) Optimization of cultural conditions for production of chitinase by Bacillus laterosporous MML2270 isolated from rice rhizosphere soil. Afr J Biotechnol 7(15):2562–2568

    CAS  Google Scholar 

  • Shinde VV, Jagtap DN, More VG, Mane MJ, Kulkarni MM (2018) Effect of n-mythelene phosponic chitosan 1.75 per cent solution on growth and yield of okra. Bioinfolet 15(3-4):274–276

    Google Scholar 

  • Sila A, Mlaik N, Sayari N, Balti R, Bougatef A (2014) Chitin and chitosan extracted from shrimp waste using fish proteases aided process: efficiency of chitosan in the treatment of unhairing effluents. J Polym Environ 22(1):78–87

    Article  CAS  Google Scholar 

  • Singh AK (2010) Optimization of culture conditions for thermostable chitinase production by Paenibacillus sp. D1. Afr J Microbiol Res 4:2291–2298

    CAS  Google Scholar 

  • Smillie RM, Krotkov G (1960) The estimation of nucleic acids in some algae and higher plants. Can J Bot 38(1):31–49

    Article  CAS  Google Scholar 

  • Stick RV, Williams SJ (2009) Disaccharides, oligosaccharides and polysaccharides. Carbohydrates: the essential molecules of life, 2nd edn. Elsevier, Oxford, pp 321–342

    Book  Google Scholar 

  • Suresh PV, Chandrasekaran M (1999) Impact of process parameters on chitinase production by an alkalophilic marine Beauveria bassiana in solid state fermentation. Process Biochem 34(3):257–267

    Article  CAS  Google Scholar 

  • Tai HS, He WH (2007) A novel composting process for plant wastes in Taiwan military barracks. Resour Conserv Recycl 51(2):408–417

    Article  Google Scholar 

  • Tsai GU, Su WH, Chen HC, Pan CL (2002) Antimicrobial activity of shrimp chitin and chitosan from different treatments. Fish Sci 68(1):170–177

    Article  CAS  Google Scholar 

  • Tsujibo H, Kubota T, Yamamoto M, Miyamoto K, Inamori Y (2003) Characterization of chitinase genes from an alkaliphilic actinomycete, Nocardiopsis prasina OPC-131. Appl Environ Microbiol 69(2):894–900

    Article  CAS  Google Scholar 

  • Vyas P, Jiwan D, Chhatpar H (2005) Statistical Optimization of Chitinase Production by Pantoea dispersa to Enhance Degradation of Crustacean Chitin Waste. J Microbiol Biotechnol 15(1):197–201

    Google Scholar 

  • Wang SL, Hwang JR (2001) Microbial reclamation of shellfish wastes for the production of chitinases. Enzym Microb Technol 28(4-5):376–382

    Article  CAS  Google Scholar 

  • Wang SL, Lin TY, Yen YH, Liao HF, Chen YJ (2006) Bioconversion of shellfish chitin wastes for the production of Bacillus subtilis W-118 chitinase. Carbohydr Res 341(15):2507–2515

    Article  CAS  Google Scholar 

  • Wang SL, Chen SJ, Wang CL (2008) Purification and characterization of chitinases and chitosanases from a new species strain Pseudomonas sp. TKU015 using shrimp shells as a substrate. Carbohydr Res 343(7):1171–1179

    Article  CAS  Google Scholar 

  • Wang SL, Hsu WH, Liang TW (2010) Conversion of squid pen by Pseudomonas aeruginosa K187 fermentation for the production of N-acetyl chitooligosaccharides and biofertilizers. Carbohydr Res 345(7):880–885

    Article  CAS  Google Scholar 

  • Winkler AJ, Dominguez-Nuñez JA, Aranaz I, Poza-Carrión C, Ramonell K, Somerville S, Berrocal-Lobo M (2017) Short-chain chitin oligomers: promoters of plant growth. Mar Drugs 15(2):40

  • Yadav M, Goswami P, Paritosh K, Kumar M, Pareek N, Vivekanand V (2019) Seafood waste: a source for preparation of commercially employable chitin/chitosan materials. Bioresour Bioprocess 6(1):8

    Article  Google Scholar 

  • Yan F, Schubert S, Mengel K (1996) Soil pH changes during legume growth and application of plant material. Biol Fertil Soils 23(3):236–242

    Article  CAS  Google Scholar 

  • Zhou J, Chen Q, Zhang Y, Fan L, Qin Z, Chen Q, Zhao L (2018) Chitooligosaccharides enhance cold tolerance by repairing photodamaged PS II in rice. J Agric Sci 156(7):888–899

    Article  CAS  Google Scholar 

  • Zou P, Li K, Liu S, Xing R, Qin Y, Yu H, Li P (2015) Effect of chitooligosaccharides with different degrees of acetylation on wheat seedlings under salt stress. Carbohydr Polym 126:62–69

    Article  CAS  Google Scholar 

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All data generated or analyzed during this study are included in this published article. The raw data retrieved during the current study are available from the corresponding author on reasonable request.

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The authors are grateful to the Department of Science & Technology and Biotechnology, Govt. of West Bengal, India for financial assistance (Memo No: 532/(Sanc.)\ST/P/S&T/2G-48/2018 dated: 27/03/2019).

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KP: sampling, investigation, formal analysis, original draft preparation; SR: methodology, visualization; KCM: supervision, review, and editing; SKH: resources, supervision, funding acquisition, conceptualization, review, and editing.

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Correspondence to Suman Kumar Halder.

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Pal, K., Rakshit, S., Mondal, K.C. et al. Microbial decomposition of crustacean shell for production of bioactive metabolites and study of its fertilizing potential. Environ Sci Pollut Res 28, 58915–58928 (2021). https://doi.org/10.1007/s11356-021-13109-z

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